Pushing to a cure by harnessing innate immunity against hepatitis C virus

Antiviral Research

Volumn 108, Issue 1, 2014, Pages 156-164

  Ireton, Reneé C ^a   Gale, Michael ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Adjuvant; Antiviral; Hepatitis C; Innate immunity; Therapeutics; Vaccine

Indexed keywords

ANTIVIRUS AGENT; DIRECT ACTING ANTIVIRUSL DRUG; HEPATITIS C VACCINE; IMMUNOMODULATING AGENT; INTERFERON; INTERFERON REGULATORY FACTOR 3; JANUS KINASE; NONSTRUCTURAL PROTEIN 3; NONSTRUCTURAL PROTEIN 4B; PROTEIN KINASE R; PROTEINASE INHIBITOR; SODIUM CHANNEL NAV1.4; STAT PROTEIN; TBK1 PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG; VIRUS PROTEIN; IMMUNOLOGIC FACTOR;

ANTIVIRAL THERAPY; COMBINATION CHEMOTHERAPY; CYTOKINE RESPONSE; DRUG TARGETING; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; IMMUNE EVASION; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREGULATION; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; VIRAL CLEARANCE; VIRUS IMMUNITY; DRUG DEVELOPMENT; DRUG EFFECTS; HEPACIVIRUS; HEPATITIS C, CHRONIC; IMMUNOLOGY; MEDICAL RESEARCH; TRENDS;

ANTIVIRAL AGENTS; BIOMEDICAL RESEARCH; DRUG DISCOVERY; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; IMMUNITY, INNATE; IMMUNOLOGIC FACTORS;

EID: 84903723133     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2014.05.012     Document Type: Note

References (112)

1. A. Aghemo, and R. De Francesco New horizons in hepatitis C antiviral therapy with direct-acting antivirals Hepatology 58 2013 428 438
2. I.C. Allen, C.B. Moore, M. Schneider, Y. Lei, B.K. Davis, M.A. Scull, D. Gris, K.E. Roney, A.G. Zimmermann, J.B. Bowzard, P. Ranjan, K.M. Monroe, R.J. Pickles, S. Sambhara, and J.P. Ting NLRX1 protein attenuates inflammatory responses to infection by interfering with the RIG-I-MAVS and TRAF6-NF-kappaB signaling pathways Immunity 34 2011 854 865
3. K. Arimoto, H. Takahashi, T. Hishiki, H. Konishi, T. Fujita, and K. Shimotohno Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125 Proc. Natl. Acad. Sci. U.S.A. 104 2007 7500 7505 (Pubitemid 47185935)
4. K. Arimoto, H. Konishi, and K. Shimotohno UbcH8 regulates ubiquitin and ISG15 conjugation to RIG-I Mol. Immunol. 45 2008 1078 1084 (Pubitemid 350016330)
5. N. Arnaud, S. Dabo, P. Maillard, A. Budkowska, K.I. Kalliampakou, P. Mavromara, D. Garcin, J. Hugon, A. Gatignol, D. Akazawa, T. Wakita, and E.F. Meurs Hepatitis C virus controls interferon production through PKR activation PLoS One 5 2010 e10575
6. N. Arnaud, S. Dabo, D. Akazawa, M. Fukasawa, F. Shinkai-Ouchi, J. Hugon, T. Wakita, and E.F. Meurs Hepatitis C virus reveals a novel early control in acute immune response PLoS Pathog. 7 2011 e1002289
7. J.S. Au, and P.J. Pockros Novel therapeutic approaches for hepatitis C Clin. Pharmacol. Ther. 95 2013 78 88
8. J.S. Au, and P.J. Pockros Novel therapeutic approaches for hepatitis C Clin. Pharmacol. Ther. 95 2013 78 88
9. P.M. Barral, D. Sarkar, Z.Z. Su, G.N. Barber, R. DeSalle, V.R. Racaniello, and P.B. Fisher Functions of the cytoplasmic RNA sensors RIG-I and MDA-5: key regulators of innate immunity Pharmacol. Ther. 124 2009 219 234
10. K.M. Bedard, M.L. Wang, S.C. Proll, Y.M. Loo, M.G. Katze, M. Gale Jr., and S.P. Iadonato Isoflavone agonists of IRF-3 dependent signaling have antiviral activity against RNA viruses J. Virol. 86 2012 7334 7344
11. P. Bellecave, M. Sarasin-Filipowicz, O. Donze, A. Kennel, J. Gouttenoire, E. Meylan, L. Terracciano, J. Tschopp, C. Sarrazin, T. Berg, D. Moradpour, and M.H. Heim Cleavage of mitochondrial antiviral signaling protein in the liver of patients with chronic hepatitis C correlates with a reduced activation of the endogenous interferon system Hepatology 51 2010 1127 1136
12. J.F. Bergmann, J. de Bruijne, D.M. Hotho, R.J. de Knegt, A. Boonstra, C.J. Weegink, A.A. van Vliet, J. van de Wetering, S.P. Fletcher, L.A. Bauman, M. Rahimy, J.R. Appleman, J.L. Freddo, H.L. Janssen, and H.W. Reesink Randomised clinical trial: anti-viral activity of ANA773, an oral inducer of endogenous interferons acting via TLR7, in chronic HCV Aliment. Pharmacol. Ther. 34 2011 443 453
13. A. Blindenbacher, F.H. Duong, L. Hunziker, S.T. Stutvoet, X. Wang, L. Terracciano, D. Moradpour, H.E. Blum, T. Alonzi, M. Tripodi, N. La Monica, and M.H. Heim Expression of hepatitis c virus proteins inhibits interferon alpha signaling in the liver of transgenic mice Gastroenterology 124 2003 1465 1475 (Pubitemid 36531819)
14. J.G. Bode, S. Ludwig, C. Ehrhardt, U. Albrecht, A. Erhardt, F. Schaper, P.C. Heinrich, and D. Haussinger IFN-alpha antagonistic activity of HCV core protein involves induction of suppressor of cytokine signaling-3 FASEB J. 17 2003 488 490
15. A. Boonstra, B.S. Liu, Z.M. Groothuismink, J.F. Bergmann, J. deBruijne, D.M. Hotho, B.E. Hansen, A.A. vanVliet, J. van de Wetering de Rooij, S.P. Fletcher, L.A. Bauman, M. Rahimy, J.R. Appleman, J.L. Freddo, H.W. Reesink, R.J. de Knegt, and H.L. Janssen Potent immune activation in chronic hepatitis C patients upon administration of an oral inducer of endogenous interferons that acts via Toll-like receptor 7 Antivir. Ther. 17 2012 657 667
16. V.C. Clark, J.A. Peter, and D.R. Nelson New therapeutic strategies in HCV: second-generation protease inhibitors Liver Int. 33 Suppl. 1 2013 80 84
17. S. Cooper, A.L. Erickson, E.J. Adams, J. Kansopon, A.J. Weiner, D.Y. Chien, M. Houghton, P. Parham, and C.M. Walker Analysis of a successful immune response against hepatitis C virus Immunity 10 1999 439 449 (Pubitemid 29205480)
18. S. Dabo, and E.F. Meurs DsRNA-dependent protein kinase PKR and its role in stress, signaling and HCV infection Viruses 4 2012 2598 2635
19. F. Diao, S. Li, Y. Tian, M. Zhang, L.G. Xu, Y. Zhang, R.P. Wang, D. Chen, Z. Zhai, B. Zhong, P. Tien, and H.B. Shu Negative regulation of MDA5- but not RIG-I-mediated innate antiviral signaling by the dihydroxyacetone kinase Proc. Natl. Acad. Sci. U.S.A. 104 2007 11706 11711 (Pubitemid 47175077)
20. M.T. Dill, F.H. Duong, J.E. Vogt, S. Bibert, P.Y. Bochud, L. Terracciano, A. Papassotiropoulos, V. Roth, and M.H. Heim Interferon-induced gene expression is a stronger predictor of treatment response than IL28B genotype in patients with hepatitis C Gastroenterology 140 2011 1021 1031
21. Q. Ding, X. Cao, J. Lu, B. Huang, Y.J. Liu, N. Kato, H.B. Shu, and J. Zhong Hepatitis C virus NS4B blocks the interaction of STING and TBK1 to evade host innate immunity J. Hepatol. 59 2013 52 58
22. F.H. Duong, M. Filipowicz, M. Tripodi, N. La Monica, and M.H. Heim Hepatitis C virus inhibits interferon signaling through up-regulation of protein phosphatase 2A Gastroenterology 126 2004 263 277 (Pubitemid 38040741)
23. M.D. Fidock, B.E. Souberbielle, C. Laxton, J. Rawal, O. Delpuech-Adams, T.P. Corey, P. Colman, V. Kumar, J.B. Cheng, K. Wright, S. Srinivasan, K. Rana, C. Craig, N. Horscroft, M. Perros, M. Westby, R. Webster, and E. van der Ryst The innate immune response, clinical outcomes, and ex vivo HCV antiviral efficacy of a TLR7 agonist (PF-4878691) Clin. Pharmacol. Ther. 89 2011 821 829
24. K.A. Fitzgerald, S.M. McWhirter, K.L. Faia, D.C. Rowe, E. Latz, D.T. Golenbock, A.J. Coyle, S.M. Liao, and T. Maniatis IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway Nat. Immunol. 4 2003 491 496 (Pubitemid 36592443)
25. E. Foy, K. Li, C. Wang, R. Sumpter Jr., M. Ikeda, S.M. Lemon, and M. Gale Jr. Regulation of interferon regulatory factor-3 by the hepatitis C virus serine protease Science 300 2003 1145 1148 (Pubitemid 36583099)
26. S. Franco, M. Parera, E. Aparicio, B. Clotet, and M.A. Martinez Genetic and catalytic efficiency structure of an HCV protease quasispecies Hepatology 45 2007 899 910 (Pubitemid 46631559)
27. S. Franco, B. Clotet, and M.A. Martinez A wide range of NS3/4A protease catalytic efficiencies in HCV-infected individuals Virus Res. 131 2008 260 270 (Pubitemid 351173398)
28. R.A. Fridell, C. Wang, J.H. Sun, D.R. O'Boyle 2nd, P. Nower, L. Valera, D. Qiu, S. Roberts, X. Huang, B. Kienzle, M. Bifano, R.E. Nettles, and M. Gao Genotypic and phenotypic analysis of variants resistant to hepatitis C virus nonstructural protein 5A replication complex inhibitor BMS-790052 in humans: in vitro and in vivo correlations Hepatology 54 2011 1924 1935
29. T. Fukuhara, A. Taketomi, T. Motomura, S. Okano, A. Ninomiya, T. Abe, H. Uchiyama, Y. Soejima, K. Shirabe, Y. Matsuura, and Y. Maehara Variants in IL28B in liver recipients and donors correlate with response to peg-interferon and ribavirin therapy for recurrent hepatitis C Gastroenterology 139 2010 1577 1585 (1585 e1-3)
30. M.U. Gack, Y.C. Shin, C.H. Joo, T. Urano, C. Liang, L. Sun, O. Takeuchi, S. Akira, Z. Chen, S. Inoue, and J.U. Jung TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity Nature 446 2007 916 920 (Pubitemid 46633167)
31. M. Gale Jr., C.M. Blakely, B. Kwieciszewski, S.L. Tan, M. Dossett, N.M. Tang, M.J. Korth, S.J. Polyak, D.R. Gretch, and M.G. Katze Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation Mol. Cell. Biol. 18 1998 5208 5218 (Pubitemid 28388104)
32. E.J. Gane, C.A. Stedman, R.H. Hyland, X. Ding, E. Svarovskaia, G.M. Subramanian, W.T. Symonds, J.G. McHutchison, and P.S. Pang Efficacy of nucleotide polymerase inhibitor sofosbuvir plus the NS5A inhibitor ledipasvir or the NS5B non-nucleoside inhibitor GS-9669 against HCV genotype 1 infection Gastroenterology 146 2013 736 743
33. U. Garaigorta, and F.V. Chisari Hepatitis C virus blocks interferon effector function by inducing protein kinase R phosphorylation Cell Host Microbe 6 2009 513 522
34. D. Ge, J. Fellay, A.J. Thompson, J.S. Simon, K.V. Shianna, T.J. Urban, E.L. Heinzen, P. Qiu, A.H. Bertelsen, A.J. Muir, M. Sulkowski, J.G. McHutchison, and D.B. Goldstein Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance Nature 461 2009 399 401
35. M.G. Ghany, D.R. Nelson, D.B. Strader, D.L. Thomas, and L.B. Seeff An update on treatment of genotype 1 chronic hepatitis C virus infection: 2011 practice guideline by the American association for the study of liver diseases Hepatology 54 2011 1433 1444
36. P. Halfon, and S. Locarnini Hepatitis C virus resistance to protease inhibitors J. Hepatol. 55 2011 192 206
37. S. Hayakawa, S. Shiratori, H. Yamato, T. Kameyama, C. Kitatsuji, F. Kashigi, S. Goto, S. Kameoka, D. Fujikura, T. Yamada, T. Mizutani, M. Kazumata, M. Sato, J. Tanaka, M. Asaka, Y. Ohba, T. Miyazaki, M. Imamura, and A. Takaoka ZAPS is a potent stimulator of signaling mediated by the RNA helicase RIG-I during antiviral responses Nat. Immunol. 12 2011 37 44
38. C.N. Hayes, M. Imamura, H. Aikata, and K. Chayama Genetics of IL28B and HCV-response to infection and treatment Nat. Rev. Gastroenterol. Hepatol. 9 2012 406 417
39. M.H. Heim, D. Moradpour, and H.E. Blum Expression of hepatitis C virus proteins inhibits signal transduction through the Jak-STAT pathway J. Virol. 73 1999 8469 8475 (Pubitemid 29441710)
40. S.M. Horner, and M. Gale Jr. Regulation of hepatic innate immunity by hepatitis C virus Nat. Med. 19 2013 879 888
41. S.M. Horner, H.M. Liu, H.S. Park, J. Briley, and M. Gale Jr. Mitochondrial-associated endoplasmic reticulum membranes (MAM) form innate immune synapses and are targeted by hepatitis C virus Proc. Natl. Acad. Sci. U.S.A. 108 2011 14590 14595
42. Y. Horsmans, T. Berg, J.P. Desager, T. Mueller, E. Schott, S.P. Fletcher, K.R. Steffy, L.A. Bauman, B.M. Kerr, and D.R. Averett Isatoribine, an agonist of TLR7, reduces plasma virus concentration in chronic hepatitis C infection Hepatology 42 2005 724 731 (Pubitemid 41233667)
43. J. Howell, P. Angus, P. Gow, and K. Visvanathan Toll-like receptors in hepatitis C infection: implications for pathogenesis and treatment J. Gastroenterol. Hepatol. 28 2013 766 776
44. C.L. Johnson, D.M. Owen, and M. Gale Jr. Functional and therapeutic analysis of hepatitis C virus NS3.4A protease control of antiviral immune defense J. Biol. Chem. 282 2007 10792 10803 (Pubitemid 47093463)
45. J.I. Kang, S.N. Kwon, S.H. Park, Y.K. Kim, S.Y. Choi, J.P. Kim, and B.Y. Ahn PKR protein kinase is activated by hepatitis C virus and inhibits viral replication through translational control Virus Res. 142 2009 51 56
46. T. Kawai, and S. Akira Toll-like receptors and their crosstalk with other innate receptors in infection and immunity Immunity 34 2011 637 650
47. T. Kawai, K. Takahashi, S. Sato, C. Coban, H. Kumar, H. Kato, K.J. Ishii, O. Takeuchi, and S. Akira IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction Nat. Immunol. 6 2005 981 988 (Pubitemid 41486182)
48. M.J. Kim, S.Y. Hwang, T. Imaizumi, and J.Y. Yoo Negative feedback regulation of RIG-I-mediated antiviral signaling by interferon-induced ISG15 conjugation J. Virol. 82 2008 1474 1483
49. A. Lahiri, P. Das, and D. Chakravortty Engagement of TLR signaling as adjuvant: towards smarter vaccine and beyond Vaccine 26 2008 6777 6783
50. B. Langhans, B. Kupfer, I. Braunschweiger, S. Arndt, W. Schulte, H.D. Nischalke, J. Nattermann, J. Oldenburg, T. Sauerbruch, and U. Spengler Interferon-lambda serum levels in hepatitis C J. Hepatol. 54 2011 859 865
51. D.T. Lau, A. Negash, J. Chen, N. Crochet, M. Sinha, Y. Zhang, J. Guedj, S. Holder, T. Saito, S.M. Lemon, B.A. Luxon, A.S. Perelson, and M.J. Gale Innate immune tolerance and the role of Kupffer cells in the differential response to interferon therapy in HCV genotype 1 patients Gastroenterology 144 2013 402 413
52. K. Li, E. Foy, J.C. Ferreon, M. Nakamura, A.C. Ferreon, M. Ikeda, S.C. Ray, M. Gale Jr., and S.M. Lemon Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF Proc. Natl. Acad. Sci. U.S.A. 102 2005 2992 2997 (Pubitemid 40299904)
53. Q. Li, A.L. Brass, A. Ng, Z. Hu, R.J. Xavier, T.J. Liang, and S.J. Elledge A genome-wide genetic screen for host factors required for hepatitis C virus propagation Proc. Natl. Acad. Sci. U.S.A. 106 2009 16410 16415
54. K. Li, N.L. Li, D. Wei, S.R. Pfeffer, M. Fan, and L.M. Pfeffer Activation of chemokine and inflammatory cytokine response in hepatitis C virus-infected hepatocytes depends on Toll-like receptor 3 sensing of hepatitis C virus double-stranded RNA intermediates Hepatology 55 2012 666 675
55. T.J. Liang Current progress in development of hepatitis C virus vaccines Nat. Med. 19 2013 869 878
56. H.M. Liu, Y.M. Loo, S.M. Horner, G.A. Zornetzer, M.G. Katze, and M. Gale Jr. The mitochondrial targeting chaperone 14-3-3epsilon regulates a RIG-I translocon that mediates membrane association and innate antiviral immunity Cell Host Microbe 11 2012 528 537
57. L. Liu, B.E. Fisher, D.L. Thomas, A.L. Cox, and S.C. Ray Spontaneous clearance of primary acute hepatitis C virus infection correlated with high initial viral RNA level and rapid HVR1 evolution Hepatology 55 2012 1684 1691
58. Y.M. Loo, and M. Gale Jr. Immune signaling by RIG-I-like receptors Immunity 34 2011 680 692
59. Y.M. Loo, D.M. Owen, K. Li, A.K. Erickson, C.L. Johnson, P.M. Fish, D.S. Carney, T. Wang, H. Ishida, M. Yoneyama, T. Fujita, T. Saito, W.M. Lee, C.H. Hagedorn, D.T. Lau, S.A. Weinman, S.M. Lemon, and M. Gale Jr. Viral and therapeutic control of IFN-beta promoter stimulator 1 during hepatitis C virus infection Proc. Natl. Acad. Sci. U.S.A. 103 2006 6001 6006
60. E. Luquin, E. Larrea, M.P. Civeira, J. Prieto, and R. Aldabe HCV structural proteins interfere with interferon-alpha Jak/STAT signalling pathway Antiviral Res. 76 2007 194 197 (Pubitemid 47410315)
61. T. Marcello, A. Grakoui, G. Barba-Spaeth, E.S. Machlin, S.V. Kotenko, M.R. MacDonald, and C.M. Rice Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics Gastroenterology 131 2006 1887 1898 (Pubitemid 44958521)
62. L.E. Markowitz, E.F. Dunne, M. Saraiya, H.W. Lawson, H. Chesson, and E.R. Unger Quadrivalent human papillomavirus vaccine: recommendations of the advisory committee on immunization practices (ACIP) MMWR Recomm. Rep. 56 2007 1 24
63. A.P. McFarland, S.M. Horner, A. Jarret, R.C. Joslyn, E. Bindewald, B.A. Shapiro, D.A. Delker, C.H. Hagedorn, M. Carrington, M. Gale Jr., and R. Savan The favorable IFNL3 genotype escapes mRNA decay mediated by AU-rich elements and hepatitis C virus-induced microRNAs Nat. Immunol. 15 2014 72 79
64. I. McGilvray, J.J. Feld, L. Chen, V. Pattullo, M. Guindi, S. Fischer, I. Borozan, G. Xie, N. Selzner, E.J. Heathcote, and K. Siminovitch Hepatic cell-type specific gene expression better predicts HCV treatment outcome than IL28B genotype Gastroenterology 142 1122-1131 2012 e1
65. P. Metz, E. Dazert, A. Ruggieri, J. Mazur, L. Kaderali, A. Kaul, U. Zeuge, M.P. Windisch, M. Trippler, V. Lohmann, M. Binder, M. Frese, and R. Bartenschlager Identification of type I and type II interferon-induced effectors controlling hepatitis C virus replication Hepatology 56 2012 2082 2093
66. M.C. Michallet, E. Meylan, M.A. Ermolaeva, J. Vazquez, M. Rebsamen, J. Curran, H. Poeck, M. Bscheider, G. Hartmann, M. Konig, U. Kalinke, M. Pasparakis, and J. Tschopp TRADD protein is an essential component of the RIG-like helicase antiviral pathway Immunity 28 2008 651 661
67. E.J. Mifsud, A.C. Tan, and D.C. Jackson TLR agonists as modulators of the innate immune response and their potential as agents against infectious disease Front. Immunol. 5 2014 79
68. P. Nakhaei, P. Genin, A. Civas, and J. Hiscott RIG-I-like receptors: sensing and responding to RNA virus infection Semin. Immunol. 21 2009 215 222
69. L.A. O'Neill Innate immunity: squelching anti-viral signalling with NLRX1 Curr. Biol. 18 2008 R302 R304
70. L.A. O'Neill, D. Golenblock, and A.G. Bowie The history of toll-like receptors- redefining innate immunity Nat. Rev. Immunol. 13 2013 453 460
71. N. Pavio, D.R. Taylor, and M.M. Lai Detection of a novel unglycosylated form of hepatitis C virus E2 envelope protein that is located in the cytosol and interacts with PKR J. Virol. 76 2002 1265 1272 (Pubitemid 34066430)
72. S. Paz, M. Vilasco, S.J. Werden, M. Arguello, D. Joseph-Pillai, T. Zhao, T.L. Nguyen, Q. Sun, E.F. Meurs, R. Lin, and J. Hiscott A functional C-terminal TRAF3-binding site in MAVS participates in positive and negative regulation of the IFN antiviral response Cell Res. 21 2011 895 910
73. P.J. Pockros New direct-acting antivirals in the development for hepatitis C virus infection Ther. Adv. Gastroenterol. 3 2010 191 202
74. Z. Raglow, C. Thoma-Perry, R. Gilroy, and Y.J. Wan IL28B genotype and the expression of ISGs in normal liver Liver Int. 33 2013 991 998
75. A. Rajput, A. Kovalenko, K. Bogdanov, S.H. Yang, T.B. Kang, J.C. Kim, J. Du, and D. Wallach RIG-I RNA helicase activation of IRF3 transcription factor is negatively regulated by caspase-8-mediated cleavage of the RIP1 protein Immunity 34 2011 340 351
76. A. Rauch, Z. Kutalik, P. Descombes, T. Cai, J. Di Iulio, T. Mueller, M. Bochud, M. Battegay, E. Bernasconi, J. Borovicka, S. Colombo, A. Cerny, J.F. Dufour, H. Furrer, H.F. Gunthard, M. Heim, B. Hirschel, R. Malinverni, D. Moradpour, B. Mullhaupt, A. Witteck, J.S. Beckmann, T. Berg, S. Bergmann, F. Negro, A. Telenti, and P.Y. Bochud Genetic variation in IL28B is associated with chronic hepatitis C and treatment failure: a genome-wide association study Gastroenterology 138 2010 1338 1345 (1345 e1-7)
77. M.D. Robek, B.S. Boyd, and F.V. Chisari Lambda interferon inhibits hepatitis B and C virus replication J. Virol. 79 2005 3851 3854 (Pubitemid 40327973)
78. C.M. Roteli-Martins, P. Naud, P. De Borba, J.C. Teixeira, N.S. De Carvalho, T. Zahaf, N. Sanchez, B. Geeraerts, and D. Descamps Sustained immunogenicity and efficacy of the HPV-16/18 AS04-adjuvanted vaccine: up to 8.4 years of follow-up Hum. Vaccine Immunother. 8 2012 390 397
79. S.M. Saalau-Bethell, A.J. Woodhead, G. Chessari, M.G. Carr, J. Coyle, B. Graham, S.D. Hiscock, C.W. Murray, P. Pathuri, S.J. Rich, C.J. Richardson, P.A. Williams, and H. Jhoti Discovery of an allosteric mechanism for the regulation of HCV NS3 protein function Nat. Chem. Biol. 8 2012 920 925
80. S.K. Saha, E.M. Pietras, J.Q. He, J.R. Kang, S.Y. Liu, G. Oganesyan, A. Shahangian, B. Zarnegar, T.L. Shiba, Y. Wang, and G. Cheng Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif EMBO J. 25 2006 3257 3263 (Pubitemid 44141784)
81. T. Saito, D.M. Owen, F. Jiang, J. Marcotrigiano, and M. Gale Jr. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA Nature 454 2008 523 527
82. M. Sarasin-Filipowicz, E.J. Oakeley, F.H. Duong, V. Christen, L. Terracciano, W. Filipowicz, and M.H. Heim Interferon signaling and treatment outcome in chronic hepatitis C Proc. Natl. Acad. Sci. U.S.A. 105 2008 7034 7039 (Pubitemid 351754525)
83. T.K. Scheel, and C.M. Rice Understanding the hepatitis C virus life cycle paves the way for highly effective therapies Nat. Med. 19 2013 837 849
84. G. Schnell, Y.M. Loo, J. Marcotrigiano, and M. Gale Jr. Uridine composition of the poly-U/UC tract of HCV RNA defines non-self recognition by RIG-I PLoS Pathog. 8 2012 e1002839
85. J.W. Schoggins, S.J. Wilson, M. Panis, M.Y. Murphy, C.T. Jones, P. Bieniasz, and C.M. Rice A diverse range of gene products are effectors of the type I interferon antiviral response Nature 472 2011 481 485
86. J.W. Schoggins, D.A. Macduff, N. Imanaka, M.D. Gainey, B. Shrestha, J.L. Eitson, K.B. Mar, R.B. Richardson, A.V. Ratushny, V. Litvak, R. Dabelic, B. Manicassamy, J.D. Aitchison, A. Aderem, R.M. Elliott, A. Garcia-Sastre, V. Racaniello, E.J. Snijder, W.M. Yokoyama, M.S. Diamond, H.W. Virgin, and C.M. Rice Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity Nature 505 2013 691 695
87. N. Sears, G.C. Sen, G.R. Stark, and S. Chattopadhyay Caspase-8-mediated cleavage inhibits IRF-3 protein by facilitating its proteasome-mediated degradation J. Biol. Chem. 286 2011 33037 33044
88. S. Sharma, B.R. tenOever, N. Grandvaux, G.P. Zhou, R. Lin, and J. Hiscott Triggering the interferon antiviral response through an IKK-related pathway Science 300 2003 1148 1151 (Pubitemid 36583100)
89. T. Shimoike, S.A. McKenna, D.A. Lindhout, and J.D. Puglisi Translational insensitivity to potent activation of PKR by HCV IRES RNA Antiviral Res. 83 2009 228 237
90. N.H. Shoukry, A. Grakoui, M. Houghton, D.Y. Chien, J. Ghrayeb, K.A. Reimann, and C.M. Walker Memory CD8+ T cells are required for protection from persistent hepatitis C virus infection J. Exp. Med. 197 2003 1645 1655 (Pubitemid 36745340)
91. F. Soares, I. Tattoli, M.E. Wortzman, D. Arnoult, D.J. Philpott, and S.E. Girardin NLRX1 does not inhibit MAVS-dependent antiviral signalling Innate Immun. 19 2013 438 448
92. C. Sommereyns, S. Paul, P. Staeheli, and T. Michiels IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo PLoS Pathog. 4 2008 e1000017
93. V. Soriano, M.G. Peters, and S. Zeuzem New therapies for hepatitis C virus infection Clin. Infect. Dis. 48 2009 313 320
94. A.E. Stone, S. Giugliano, G. Schnell, L. Cheng, K.F. Leahy, L. Golden-Mason, M. Gale Jr., and H.R. Rosen Hepatitis C virus pathogen associated molecular pattern (PAMP) triggers production of lambda-interferons by human plasmacytoid dendritic cells PLoS Pathog. 9 2013 e1003316
95. A.I. Su, J.P. Pezacki, L. Wodicka, A.D. Brideau, L. Supekova, R. Thimme, S. Wieland, J. Bukh, R.H. Purcell, P.G. Schultz, and F.V. Chisari Genomic analysis of the host response to hepatitis C virus infection Proc. Natl. Acad. Sci. U.S.A. 99 2002 15669 15674 (Pubitemid 35403989)
96. V. Suppiah, M. Moldovan, G. Ahlenstiel, T. Berg, M. Weltman, M.L. Abate, M. Bassendine, U. Spengler, G.J. Dore, E. Powell, S. Riordan, D. Sheridan, A. Smedile, V. Fragomeli, T. Muller, M. Bahlo, G.J. Stewart, D.R. Booth, and J. George IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy Nat. Genet. 41 2009 1100 1104
97. F. Takeshita, K. Kobiyama, A. Miyawaki, N. Jounai, and K. Okuda The non-canonical role of Atg family members as suppressors of innate antiviral immune signaling Autophagy 4 2008 67 69
98. Y. Tanaka, N. Nishida, M. Sugiyama, M. Kurosaki, K. Matsuura, N. Sakamoto, M. Nakagawa, M. Korenaga, K. Hino, S. Hige, Y. Ito, E. Mita, E. Tanaka, S. Mochida, Y. Murawaki, M. Honda, A. Sakai, Y. Hiasa, S. Nishiguchi, A. Koike, I. Sakaida, M. Imamura, K. Ito, K. Yano, N. Masaki, F. Sugauchi, N. Izumi, K. Tokunaga, and M. Mizokami Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C Nat. Genet. 41 2009 1105 1109
99. A.W. Tarr, R.A. Urbanowicz, and J.K. Ball The role of humoral innate immunity in hepatitis C virus infection Viruses 4 2012 1 27
100. K.E. Taylor, and K.L. Mossman Recent advances in understanding viral evasion of type I interferon Immunology 138 2013 190 197
101. D.R. Taylor, S.T. Shi, P.R. Romano, G.N. Barber, and M.M. Lai Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein Science 285 1999 107 110 (Pubitemid 29307576)
102. R. Thimme, M. Binder, and R. Bartenschlager Failure of innate and adaptive immune responses in controlling hepatitis C virus infection FEMS Microbiol. Rev. 36 2012 663 683
103. D.L. Thomas, C.L. Thio, M.P. Martin, Y. Qi, D. Ge, C. O'Huigin, J. Kidd, K. Kidd, S.I. Khakoo, G. Alexander, J.J. Goedert, G.D. Kirk, S.M. Donfield, H.R. Rosen, L.H. Tobler, M.P. Busch, J.G. McHutchison, D.B. Goldstein, and M. Carrington Genetic variation in IL28B and spontaneous clearance of hepatitis C virus Nature 461 2009 798 801
104. D. Uzri, and L. Gehrke Nucleotide sequences and modifications that determine RIG-I/RNA binding and signaling activities J. Virol. 83 2009 4174 4184
105. C.M. Walker Adaptive immunity to the hepatitis C virus Adv. Virus Res. 78 2010 43 86
106. N. Wang, Y. Liang, S. Devaraj, J. Wang, S.M. Lemon, and K. Li Toll-like receptor 3 mediates establishment of an antiviral state against hepatitis C virus in hepatoma cells J. Virol. 83 2009 9824 9834
107. E. Wies, M.K. Wang, N.P. Maharaj, K. Chen, S. Zhou, R.W. Finberg, and M.U. Gack Dephosphorylation of the RNA sensors RIG-I and MDA5 by the phosphatase PP1 is essential for innate immune signaling Immunity 38 2013 437 449
108. K. Witte, E. Witte, R. Sabat, and K. Wolk IL-28A, IL-28B, and IL-29: promising cytokines with type I interferon-like properties Cytokine Growth Factor Rev. 21 2010 237 251
109. P.L. Yang, M. Gao, K. Lin, Q. Liu, and V.A. Villareal Anti-HCV drugs in the pipeline Curr. Opin. Virol. 1 2011 607 616
110. R. Yoshida, G. Takaesu, H. Yoshida, F. Okamoto, T. Yoshioka, Y. Choi, S. Akira, T. Kawai, A. Yoshimura, and T. Kobayashi TRAF6 and MEKK1 play a pivotal role in the RIG-I-like helicase antiviral pathway J. Biol. Chem. 283 2008 36211 36220
111. C.I. Yu, and B.L. Chiang A new insight into hepatitis C vaccine development J. Biomed. Biotechnol. 2010 2010 548280
112. W. Zeng, L. Sun, X. Jiang, X. Chen, F. Hou, A. Adhikari, M. Xu, and Z.J. Chen Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity Cell 141 2010 315 330